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Pollinators and nectar robbers cause directional selection for large spur circle in Impatiens oxyanthera (Balsaminaceae)

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Abstract

Nectar spurs have an important role in floral evolution and plant–pollinator coadaptation. The flowers of some species possess spurs curving into a circle. However, it is unclear whether spur circle diameter is under direct selection pressure from different sources, such as pollinators and nectar robbers. In this study, we quantified selection on some floral traits, such as spur circle diameter in Impatiens oxyanthera (Balsaminaceae) using phenotypic selection analysis and compared the relative importance of pollinators and nectar robbers as selective agents using mediation analysis. The study showed that pollinators caused significant selection on corolla length, spur curvature and spur circle diameter while nectar robbers only imposed strong selection on spur circle diameter. Pollinators favored flowers with large corolla, curly spurs and large spur circle while nectar robbers preferred flowers with small spur circle. More pollinator visits resulted in higher female reproductive success, while robbery reduced female fitness. Conflicting selection on spur traits from pollinators and nectar robbers was not found. Mediation analysis showed that selection on floral traits through nectar robbing was stronger than selection through pollination. The results suggested that pollinators and nectar robbers jointly mediated the directional selection for large spur circle, and nectar robbers caused stronger selection than pollinators on floral traits.

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References

  • Alexandersson R, Johnson SD (2002) Pollinator-mediated selection on flower-tube length in a hawkmoth-pollinated Gladiolus (Iridaceae). Proc R Soc Lond B 269:631–636

    Article  Google Scholar 

  • Ashman TL, Penet L (2007) Direct and indirect effects of a sex-biased antagonist on male and female fertility: consequences for reproductive trait evolution in a gender-dimorphic plant. Am Nat 169:595–608

    Article  PubMed  Google Scholar 

  • Bartkowska MP, Johnston MO (2012) Pollinators cause stronger selection than herbivores on floral traits in Lobelia cardinalis (Lobeliaceae). New Phytol 193:1039–1048

    Article  PubMed  Google Scholar 

  • Boberg E, Ågren J (2009) Despite their apparent integration, spur length but not perianth size affects reproductive success in the moth-pollinated orchid Platanthera bifolia. Funct Ecol 23:1022–1028

    Article  Google Scholar 

  • Brody AK (1992) Oviposition choices by a predispersal seed predator (Hylemya sp). I. Correspondence with hummingbird pollinators, and the role of plant size, density and floral morphology. Oecologia 91:56–62

    Google Scholar 

  • Brody AK, Irwin RE, McCutcheon ML, Parsons EC (2008) Interactions between nectar robbers and seed predators mediated by a shared host plant, Ipomopsis aggregata. Oecologia 155:75–84

    Article  PubMed  Google Scholar 

  • Brunet J (2009) Pollinators of the Rocky Mountain columbine: temporal variation, functional groups and associations with floral traits. Ann Bot 103:1567–1578

    Article  PubMed  Google Scholar 

  • Burkle LA, Irwin RE, Newman DA (2007) Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system. Am J Bot 94:1935–1943

    Article  PubMed  Google Scholar 

  • Campbell DR, Waser NM, Price MV (1996) Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata. Ecology 77:1463–1472

    Article  Google Scholar 

  • Cariveau D, Irwin RE, Brody AK, Garcia-Mayeya LS, von der Ohe A (2004) Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits. Oikos 104:15–26

    Article  Google Scholar 

  • Carpenter FL (1979) Competition between hummingbirds and insects for nectar. Amer Zool 19:1105–1114

    Google Scholar 

  • Caruso CM, Remington DLD, Ostergren KE (2005) Variation in resource limitation of plant reproduction influences natural selection on floral traits of Asclepias syriaca. Oecologia 146:68–76

    Article  PubMed  Google Scholar 

  • Castro S, Silveira P, Navarro L (2008) Consequences of nectar robbing for the fitness of a threatened plant species. Plant Ecol 199:201–208

    Article  Google Scholar 

  • Chen YL (2001) Flora Reipublicae Popularis Sinicae. Tomus, vol 47, no 2. Science Press, Beijing, pp 142–143

    Google Scholar 

  • Conner JK (1988) Field measurements of natural and sexual selection in the fungus beetle, Bolitotherus cornutus. Evolution 42:736–749

    Article  Google Scholar 

  • Cuartas-Domínguez M, Medel R (2010) Pollinator-mediated selection and experimental manipulation of the flower phenotype in Chloraea bletioides. Funct Ecol 24:1219–1227

    Article  Google Scholar 

  • Deng XB, Ren PY, Gao JY, Li QJ (2004) The striped squirrel (Tamiops swinhoei hainanus) as a nectar robber of ginger (Alpinia kwangsiensis). Biotropica 36:633–636

    Google Scholar 

  • Ellis AG, Johnson SD (2010) Gender differences in the effects of floral spur length manipulation on fitness in a hermaphrodite orchid. Int J Plant Sci 171:1010–1019

    Article  Google Scholar 

  • Fenster CB, Cheely G, Dudash MR, Reynolds RJ (2006) Nectar reward and advertisement in hummingbird-pollinated Silene virginica (Caryophyllaceae). Am J Bot 93:1800–1807

    Article  PubMed  Google Scholar 

  • Fishman L, Willis JH (2008) Pollen limitation and natural selection on floral characters in the yellow monkeyflower, Mimulus guttatus. New Phytol 177:802–810

    Article  PubMed  Google Scholar 

  • Galen C (1989) Measuring pollinator-mediated selection on morphometric floral traits: bumblebees and the alpine sky pilot, Polemonium viscosum. Evolution 43:882–890

    Article  Google Scholar 

  • Galen C, Cuba J (2001) Down the tube: pollinators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium viscosum. Evolution 55:1963–1971

    PubMed  CAS  Google Scholar 

  • Gómez JM (2003) Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. Am Nat 162:242–256

    Article  PubMed  Google Scholar 

  • Gómez JM, Bosch J, Perfectti F, Fernández JD, Abdelaziz M, Camacho JPM (2008) Association between floral traits and rewards in Erysimum mediohispanicum (Brassicaceae). Ann Bot 101:1413–1420

    Article  PubMed  Google Scholar 

  • Gómez JM, Abdelaziz M, Muñoz-Pajares J, Perfectti F (2009) Heritability and genetic correlation of corolla shape and size in Erysimum mediohispanicum. Evolution 63:1820–1831

    Article  PubMed  Google Scholar 

  • Gong YB, Huang SQ (2009) Floral symmetry: pollinator-mediated stabilizing selection on flower size in bilateral species. Proc R Soc B 276:4013–4020

    Article  PubMed  Google Scholar 

  • Grace JB, Pugesek BH (1998) On the use of path analysis and related procedures for the investigation of ecological problems. Am Nat 152:151–159

    Article  PubMed  CAS  Google Scholar 

  • Hodges SA (1997) Floral nectar spurs and diversification. Int J Plant Sci 158:S81–S88

    Article  Google Scholar 

  • Hodges SA, Arnold ML (1995) Spurring plant diversification: are floral nectar spurs a key innovation? Proc R Soc Lond B 262:343–348

    Article  Google Scholar 

  • Institute of Soil Science, Chinese Academy of Science (1978) Analysis of soil physical and chemical properties. Shanghai Science and Technology Press, Shanghai

    Google Scholar 

  • Irwin RE (2006) The consequences of direct versus indirect species interactions to selection on traits: pollination and nectar robbing in Ipomopsis aggregata. Am Nat 167:315–328

    Article  PubMed  Google Scholar 

  • Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116:519–527

    Article  Google Scholar 

  • Irwin RE, Brody AK (1999) Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregata (Polemoniaceae). Ecology 80:1703–1712

    Google Scholar 

  • Irwin RE, Brody AK (2000) Consequences of nectar robbing for realized male function in a hummingbird-pollinated plant. Ecology 81:2637–2643

    Article  Google Scholar 

  • Irwin RE, Maloof JE (2002) Variation in nectar robbing over time, space, and species. Oecologia 133:525–533

    Article  Google Scholar 

  • Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol S 41:271–292

    Article  Google Scholar 

  • Jennersten O, Nilsson SG (1993) Insect flower visitation frequency and seed production in relation to patch size of Viscaria vulgaris (Caryophyllaceae). Oikos 68:283–292

    Article  Google Scholar 

  • Johnson SD, Steiner KE (1997) Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchidaceae). Evolution 51:45–53

    Article  Google Scholar 

  • Kato M (1988) Bumblebee visits to Impatiens spp.: pattern and efficiency. Oecologia 76:364–370

    Google Scholar 

  • Kingsolver JG, Schemske DW (1991) Path analyses of selection. Trends Ecol Evol 6:276–280

    Article  PubMed  CAS  Google Scholar 

  • Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261

    Article  PubMed  CAS  Google Scholar 

  • Knight TM (2003) Floral density, pollen limitation, and reproductive success in Trillium grandiflorum. Oecologia 442:557–563

    Article  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  Google Scholar 

  • Lara C, Ornelas JF (2001) Preferential nectar robbing of flowers with long corollas: experimental studies of two hummingbird species visiting three plant species. Oecologia 128:263–273

    Article  Google Scholar 

  • Lavergne S, Debussche M, Thompson JD (2005) Limitations on reproductive success in endemic Aquilegia viscosa (Ranunculaceae) relative to its widespread congener Aquilegia vulgaris: the interplay of herbivory and pollination. Oecologia 142:212–220

    Article  PubMed  Google Scholar 

  • Little KJ, Dieringer G, Romano M (2005) Pollination ecology, genetic diversity and selection on nectar spur length in Platanthera lacera (Orchidaceae). Plant Spec Biol 20:183–190

    Article  Google Scholar 

  • Liu KF (1992) A study on climate in Mt. Emei. J Mianyang Agricultural College 9:44–48

    Google Scholar 

  • Liu L, Wu W, Zheng YL, Huang CY, Liu RJ (2007) Variations on the chemical components of the volatile oil of Houttuynia cordata Thunb. populations from different valleys and altitudes of Mt. Emei. Acta Ecologica Sinica 27:2239–2250

    Article  CAS  Google Scholar 

  • Lu YQ (1988) Systematic study on Impatiens L. (Balsaminaceae) of Mt. Emei and referring to the variations within Balsaminaceae. Master degree thesis, Institute of Botany, Chinese Academy of Sciences, pp 8–9

  • Lu RK (2000) Analysis methods of soil agricultural chemistry. China Agricultural Science and Technology Press, Beijing

    Google Scholar 

  • Maloof JE (2001) The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am J Bot 88:1960–1965

    Article  PubMed  CAS  Google Scholar 

  • Mao ZB, Boehler C, Ge XJ (2011) Pollination ecology and breeding system of Impatiens lateristachys (Balsaminaceae) endemic to China. Guihaia 31:160–166

    Google Scholar 

  • Mitchell RJ (1993) Adaptive significance of Ipomopsis aggregata nectar production: observation and experiment in the field. Evolution 47:25–35

    Article  Google Scholar 

  • Mitchell RJ (1994) Effects of floral traits, pollinator visitation, and plant size on Ipomopsis aggregata fruit production. Am Nat 143:870–889

    Article  Google Scholar 

  • Moré M, Amorim FW, Benitez-Vieyra S, Medina AM, Sazima M, Cocucci AA (2012) Armament imbalances: match and mismatch in plant–pollinator traits of highly specialized long-spurred orchids. PLoS ONE 7:e41878

    Article  PubMed  Google Scholar 

  • Navarro L (2001) Reproductive biology and effect of nectar robbing on fruit production in Macleania bullata (Ericaceae). Plant Ecol 152:59–65

    Article  Google Scholar 

  • Navarro L, Medel R (2009) Relationship between floral tube length and nectar robbing in Duranta erecta L. (Verbenaceae). Biol J Linn Soc 96:392–398

    Article  Google Scholar 

  • Newman DA, Thomson JD (2005) Effects of nectar robbing on nectar dynamics and bumblebee foraging strategies in Linaria vulgaris (Scrophulariaceae). Oikos 110:309–320

    Article  Google Scholar 

  • Pan IL (1999) Pollinator-mediated selection on a floral trait: spur variation in Impatiens capensis. Senior honors thesis. Department of Biology, Amherst College, Amherst

  • Parachnowitsch AL, Caruso CM (2008) Predispersal seed herbivores, not pollinators, exert selection on floral traits via female fitness. Ecology 89:1802–1810

    Article  PubMed  Google Scholar 

  • Parachnowitsch AL, Kessler A (2010) Pollinators exert natural selection on flower size and floral display in Penstemon digitalis. New Phytol 188:393–402

    Article  PubMed  Google Scholar 

  • Preacher KJ, Hayes AF (2008) Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav Res Methods 40:879–891

    Article  PubMed  Google Scholar 

  • Pyke GH (1991) What does it cost a plant to produce floral nectar? Nature 350:58–59

    Article  Google Scholar 

  • Rust RW (1977) Pollination in Impatiens capensis and Impatiens pallida (Balsaminaceae). Bull Torrey Bot Club 104:361–367

    Article  Google Scholar 

  • Sánchez-Lafuente AM (2007) Corolla herbivory, pollination success and fruit predation in complex flowers: an experimental study with Linaria lilacina (Scrophulariaceae). Ann Bot 99:355–364

    Article  PubMed  Google Scholar 

  • Sandring S, Ågren J (2009) Pollinator-mediated selection on floral display and flowering time in the perennial herb Arabidopsis lyrata. Evolution 63:1292–1300

    Article  PubMed  Google Scholar 

  • Sletvold N, Ågren J (2010) Pollinator-mediated selection on floral display and spur length in the orchid Gymnadenia conopsea. Int J Plant Sci 171:999–1009

    Article  Google Scholar 

  • Sletvold N, Ågren J (2011) Nonadditive effects of floral display and spur length on reproductive success in a deceptive orchid. Ecology 92:2167–2174

    Article  PubMed  Google Scholar 

  • Sletvold N, Grindeland JM, Ågren J (2010) Pollinator-mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica. New Phytol 188:385–392

    Article  PubMed  Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol S 35:435–466

    Article  Google Scholar 

  • Temeles EJ, Pan IL (2002) Effect of nectar robbery on phase duration, nectar volume, and pollination in a protandrous plant. Int J Plant Sci 163:803–808

    Article  Google Scholar 

  • Tian JP, Liu KM, Hu GW (2004) Pollination ecology and pollination system of Impatiens reptans (Balsaminaceae) endemic to China. Ann Bot 93:167–175

    Article  PubMed  Google Scholar 

  • Totland Ø (2001) Environment-dependent pollen limitation and selection on floral traits in an alpine species. Ecology 82:2233–2244

    Article  Google Scholar 

  • Totland Ø, Andersen HL, Bjelland T, Dahl V, Eide W, Houge S, Pedersen TR, Vie EU (1998) Variation in pollen limitation among plants and phenotypic selection on floral traits in an early-spring flowering herb. Oikos 82:491–501

    Article  Google Scholar 

  • Travers SE, Temeles EJ, Pan I (2003) The relationship between nectar spur curvature in jewelweed (Impatiens capensis) and pollen removal by hummingbird pollinators. Can J Bot 81:164–170

    Article  Google Scholar 

  • Urcelay C, Morales CL, Chalcoff VR (2006) Relationship between corolla length and floral larceny in the South American hummingbird-pollinated Campsidium valdivianum (Bignoniaceae). Ann Bot Fenn 43:205–211

    Google Scholar 

  • Wang Y (2008) Collection and preservation of Impatiens spp. Doctor degree thesis, Beijing Forestry University

    Google Scholar 

  • Wen ZL, Chang L, Hau KT, Liu HY (2004) Testing and application of the mediating effects. Acta Psychologica Sinica 36:614–620

    Google Scholar 

  • Whittall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706–709

    Article  PubMed  CAS  Google Scholar 

  • Wilson P (1995) Selection for pollination success and the mechanical fit of Impatiens flowers around bumblebee bodies. Biol J Linn Soc 55:355–383

    Google Scholar 

  • Xiao LX (2009) The pollination biology of four species of Impatiens L. Master degree thesis, Hunan Normal University

  • Yang CF, Guo YH (2004) Pollen size–number trade-off and pollen-pistil relationships in Pedicularis (Orobanchaceae). Plant Syst Evol 247:177–185

    Article  Google Scholar 

  • Young HJ (2008) Selection on spur shape in Impatiens capensis. Oecologia 156:535–543

    Article  PubMed  Google Scholar 

  • Young HJ, Dunning DW, von Hasseln KW (2007) Foraging behavior affects pollen removal and deposition in Impatiens capensis (Balsaminaceae). Am J Bot 94:1267–1271

    Article  PubMed  Google Scholar 

  • Zhang YW, Robert GW, Wang Y, Guo YH (2007) Nectar robbing of a carpenter bee and its effects on the reproductive fitness of Glechoma longituba (Lamiaceae). Plant Ecol 193:1–13

    Article  Google Scholar 

  • Zhang YW, Zhao JM, Yang CF, Gituru WR (2011) Behavioural differences between male and female carpenter bees in nectar robbing and its effect on reproductive success in Glechoma longituba (Lamiaceae). Plant Biol 13:25–32

    Article  PubMed  Google Scholar 

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Acknowledgments

We are very grateful to Dr. Zeqing Niu, Dr. Aimin Shi and Prof. Min Wang for identifying insects; Prof. Fake Zheng for taking photos of insect specimens; Prof. Yingqing Lu and Mr. Cehong Li for identifying target species; Dong Wang, Chaoying Cai, Guoyi He, Xiange Cheng, Fushuo Huang, Hui Gao, Fupan Wang, Pei Xiong and Chuan Wan for help in the field; Dr. Jinsong Chen, Huajun Yin, Qiumei Quan, Zhenfeng Xu, and Lei Gu for valuable comments on the manuscript; Mr. Ping Zhou and Miss. Jin He for support; Hong Wang for drawing; Youyou Huang for calculating the distance between plots; Aiying Shen and Ronghua Wang for editing language, and two reviewers for comments on an earlier version of this manuscript. This work was supported jointly by the “Strategic Priority Research Program—Climate Change: Carbon Budget and Relevant Issues” of the Chinese Academy of Sciences (XD A01050303), the National Natural Science Foundation of China (31270552) and the National Key Technology R&D Program (2011BAC09B04).

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Wang, Q., Li, Y., Pu, X. et al. Pollinators and nectar robbers cause directional selection for large spur circle in Impatiens oxyanthera (Balsaminaceae). Plant Syst Evol 299, 1263–1274 (2013). https://doi.org/10.1007/s00606-013-0794-x

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